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First published online August 7, 2009; 10.1104/pp.109.139733 Plant Physiology 151:955-965 (2009) © 2009 American Society of Plant Biologists
Ectopic 5' Splice Sites Inhibit Gene Expression by Engaging RNA Surveillance and Silencing Pathways in Plants1,[C],[W]Plant Pathology Department, Scottish Crop Research Institute, Invergowrie DD2 5DA, United Kingdom (K.W., C.H., J.A.S., J.S., C.L.); Department of Molecular Biology and Biochemistry, Rutgers University, State University of New Jersey, Piscataway, New Jersey 08854 (R.G., S.I.G.); Institute of Molecular Plant Sciences, University of Edinburgh, Edinburgh EH9 3JR, United Kingdom (C.L.); and Science and Advice for Scottish Agriculture, Virology and Zoology Section, Edinburgh EH12 9FJ, United Kingdom (C.L.)
The quality control of mRNA maturation is a highly regulated process that surveys pre-mRNA integrity and eliminates improperly matured pre-mRNAs. In nature, certain viruses regulate the expression of their genes by hijacking the endogenous RNA quality control machinery. We demonstrate that the inclusion of 5' splice sites within the 3'-untranslated region of a reporter gene in plants alters the pre-mRNA cleavage and polyadenylation process, resulting in pre-mRNA degradation, exemplifying a regulatory mechanism conserved between kingdoms. Altered pre-mRNA processing was associated with an inhibition of homologous gene expression in trans and the preferential accumulation of 24-nucleotide (nt) short-interfering RNAs (siRNAs) as opposed to 21-nt siRNA subspecies, suggesting that degradation of the aberrant pre-mRNA involves the silencing machinery. However, gene expression was not restored by coexpression of a silencing suppressor or in an RNA-dependent RNA polymerase (RDR6)-deficient background despite reduced 24-nt siRNA accumulation. Our data highlight a complex cross talk between the quality control RNA machinery, 3'-end pre-mRNA maturation, and RNA-silencing pathways capable of discriminating among different types of aberrant RNAs.
1 This work was supported by the Rainbow Seed Fund (to C.L., K.W., J.S.), Scottish Enterprise (C.L.), and the Scottish Government Rural and Environment Research and Analysis Directorate (to C.L., J.A.S.). K.W. and C.H. were the recipients of a Marie Curie Intra-European Fellowship (grant nos. MEIF–CT–2005–515334 and MEIF–CT–2005–025076, respectively). S.I.G. and R.G. were supported by National Institutes of Health grants (grant nos. GM57286 [to S.I.G.] and CA119934 [to S.I.G.]). 2 Present address: The Institute of Cardiovascular Research, University of Dundee, Dundee DD1 9SY, UK. 3 Present address: Genetics Programme, Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, UK. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Christophe Lacomme (christophe.lacomme{at}sasa.gsi.gov.uk). [C] Some figures in this article are displayed in color online but in black and white in the print edition. [W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.109.139733 * Corresponding author; e-mail christophe.lacomme{at}sasa.gsi.gov.uk. Received April 8, 2009; accepted August 4, 2009; published August 7, 2009.
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